Ecological Monographs, 76(4), 2006, pp. 521–547 Ó 2006 by the Ecological Society of America TOLERANCE TO SHADE, DROUGHT, AND WATERLOGGING OF TEMPERATE NORTHERN HEMISPHERE TREES AND SHRUBS U ¨ LO NIINEMETS 1,2 AND FERNANDO VALLADARES 3,4 1 Department of Plant Physiology, University of Tartu, Riia 23, 51011 Tartu, Estonia 2 Centro di Ecologia Alpina, I-38040 Viote del Monte Bondone (TN), Italy 3 Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, C.S.I.C., Serrano 115 dpdo., E-28006 Madrid, Spain Abstract. Lack of information on ecological characteristics of species across different continents hinders development of general world-scale quantitative vegetation dynamic models. We constructed common scales of shade, drought, and waterlogging tolerance for 806 North American, European/West Asian, and East Asian temperate shrubs and trees representing about 40% of the extant natural Northern Hemisphere species pool. These scales were used to test the hypotheses that shade tolerance is negatively related to drought and waterlogging tolerances, and that these correlations vary among continents and plant functional types. We observed significant negative correlations among shade and drought tolerance rankings for all data pooled, and separately for every continent and plant functional type, except for evergreen angiosperms. Another significant trade-off was found for drought and waterlogging tolerance for all continents, and for evergreen and deciduous angiosperms, but not for gymnosperms. For all data pooled, for Europe and East Asia, and for evergreen and deciduous angiosperms, shade tolerance was also negatively associated with waterlogging tolerance. Quantile regressions revealed that the negative relationship between shade and drought tolerance was significant for species growing in deep to moderate shade and that the negative relationship between shade and waterlogging tolerance was significant for species growing in moderate shade to high light, explaining why all relationships between different tolerances were negative according to general regression analyses. Phylogenetic signal in the tolerance to any one of the three environmental factors studied was significant but low, with only 21–24% of cladogram nodes exhibiting significant conservatism. The inverse relationships between different tolerances were significant in phylogenetically independent analyses both for the overall pool of species and for two multispecies genera (Pinus and Quercus) for which reliable molecular phylogenies were available. Only 2.6–10.3% of the species were relatively tolerant to two environmental stresses simultaneously (tolerance value 3), and only three species were tolerant to all three stresses, supporting the existence of functional trade-offs in adjusting to multiple environmental limitations. These trade-offs represent a constraint for niche differentiation, reducing the diversity of plant responses to the many combinations of irradiance and water supply that are found in natural ecosystems. Key words: drought tolerance; functional plant type; intercontinental comparisons; phylogeny; shade tolerance; trade-offs; waterlogging tolerance. INTRODUCTION Differential tolerance to environmental stress among plants is a crucial aspect underlying geographic patterns of vegetation and a central concept to understanding the structure and dynamics of terrestrial ecosystems (Moo- ney et al. 2002). Tolerance to a given stress has a physiological basis but it is strongly affected by many environmental factors, which has led to the distinction between physiological and ecological tolerances. The tolerance to a given stress is typically reduced by other co-occurring stresses or by biotic factors such as herbivores, pests, and competition from neighbor plants. For example shade tolerance is reduced by mildew in many temperate forest species such as oaks (Rackham 2003), and by drought in woody seedlings (Battaglia et al. 2000, Sa´nchez-Go´ mez et al. 2006b). However, knowledge of the tolerance to the primary abiotic stresses is still scant for many important wild plants and tolerance to simultaneous stresses is poorly under- stood despite the ubiquitous coexistence of multiple stresses in nature (Hall and Harcombe 1998, Battaglia et al. 2000, Niinemets and Valladares 2004). Due at least in part to these knowledge gaps, few attempts have been made to develop a general theory of succession and dynamics for main vegetation types across the globe, and the existing diversity of theories on vegetation dynamics is associated with the lack of a common intercontinental stress tolerance scale (Bugmann and Solomon 1995, Bugmann and Cramer 1998, Peng 2000, Glenz 2005). Manuscript received 17 October 2005; revised and accepted 22 December 2005; final version received 9 April 2006. Corresponding Editor: M. J. Lechowicz. 4 Corresponding author. E-mail: [email protected]521
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Ecological Monographs, 76(4), 2006, pp. 521–547� 2006 by the Ecological Society of America
TOLERANCE TO SHADE, DROUGHT, AND WATERLOGGING OFTEMPERATE NORTHERN HEMISPHERE TREES AND SHRUBS
ULO NIINEMETS1,2
AND FERNANDO VALLADARES3,4
1Department of Plant Physiology, University of Tartu, Riia 23, 51011 Tartu, Estonia2Centro di Ecologia Alpina, I-38040 Viote del Monte Bondone (TN), Italy
3Instituto de Recursos Naturales, Centro de Ciencias Medioambientales, C.S.I.C., Serrano 115 dpdo., E-28006 Madrid, Spain
Abstract. Lack of information on ecological characteristics of species across differentcontinents hinders development of general world-scale quantitative vegetation dynamicmodels. We constructed common scales of shade, drought, and waterlogging tolerance for 806North American, European/West Asian, and East Asian temperate shrubs and treesrepresenting about 40% of the extant natural Northern Hemisphere species pool. Thesescales were used to test the hypotheses that shade tolerance is negatively related to droughtand waterlogging tolerances, and that these correlations vary among continents and plantfunctional types. We observed significant negative correlations among shade and droughttolerance rankings for all data pooled, and separately for every continent and plant functionaltype, except for evergreen angiosperms. Another significant trade-off was found for droughtand waterlogging tolerance for all continents, and for evergreen and deciduous angiosperms,but not for gymnosperms. For all data pooled, for Europe and East Asia, and for evergreenand deciduous angiosperms, shade tolerance was also negatively associated with waterloggingtolerance. Quantile regressions revealed that the negative relationship between shade anddrought tolerance was significant for species growing in deep to moderate shade and that thenegative relationship between shade and waterlogging tolerance was significant for speciesgrowing in moderate shade to high light, explaining why all relationships between differenttolerances were negative according to general regression analyses. Phylogenetic signal in thetolerance to any one of the three environmental factors studied was significant but low, withonly 21–24% of cladogram nodes exhibiting significant conservatism. The inverse relationshipsbetween different tolerances were significant in phylogenetically independent analyses both forthe overall pool of species and for two multispecies genera (Pinus and Quercus) for whichreliable molecular phylogenies were available. Only 2.6–10.3% of the species were relativelytolerant to two environmental stresses simultaneously (tolerance value �3), and only threespecies were tolerant to all three stresses, supporting the existence of functional trade-offs inadjusting to multiple environmental limitations. These trade-offs represent a constraint forniche differentiation, reducing the diversity of plant responses to the many combinations ofirradiance and water supply that are found in natural ecosystems.
Asian, and 23% of East Asian woody species; Qian and
Ricklefs 1999, 2000, Ricklefs et al. 2004).
Construction of uniform tolerance rankings
for Northern Hemisphere
Shade, drought, and waterlogging tolerance rankings
of species were first developed separately for every
continent using an extensive selection of published
tolerance rankings, and cross-calibrating every tolerance
ranking using species present in several tolerance
rankings. The continent-specific rankings were further
converted to word-scale shade, drought, and water-
logging rankings using tolerance estimates for more than
a hundred native and introduced widespread species that
were available for two or more continents (Figs. 1, 2).
Data from different sources and different environmental
conditions led to different rankings of tolerance for a
given species. Here we use the average, always after
detailed cross-calibration of the different data sets using
common species. The standard error, which is given for
species with rankings available from two or more studies
(Appendix A), reflects this dispersion. To control for
erroneous data, estimates of the species requirement in
any single data set that differed by more than two levels
from the general species mean were removed, and the
corrected species mean value was calculated. Basic steps
followed for the cross-calibration among different
sources are given in the following section; a more
detailed description of the process followed to get a
common scale of tolerance and a list of the original
sources of information are provided in Appendix B.
Derivation of shade tolerance scales
From the many possible definitions of shade tolerance
(survival, growth, completion of life cycle, optimal
physiological performance, etc.; e.g., Grime 1979, Smith
and Huston 1989, Woodward 1990, Grubb 1998, Reich
et al. 2003, Valladares et al. 2005a), shade tolerance is
taken here as the capacity for growth in the shade. Since
shade comprises a range of light availabilities from very
dark to rather bright environments, shade tolerance is
ideally defined by the minimum light at which a given
species is able to grow. Shade tolerance of woody plants
is most frequently provided for the juveniles of each
species and thus the values obtained here apply
primarily to seedlings and saplings. Even though many
species have been shown to change their shade tolerance
during their lifetime, with a tendency for a decreasing
tolerance with age, in most cases the relative rankings of
FIG. 1. (A) Relationships between the shade tolerance scoring developed for temperate species in North America and thespecies light requirement developed in Europe (Ellenberg’s light indicator value; Ellenberg 1991), and (B) relationships between theNorth American shade tolerance ranking and the species scoring developed in East Asia. Data points in (A) correspond to native,naturalized, or widely occurring species in both North America and Europe. In (B), the shade tolerance estimates derived forintroduced East Asian species in North America and Europe are regressed against the shade tolerance estimates determined for thesame species growing in the native habitats in East Asia. The dashed line in (B) denotes the 1:1 relationship. The correlation in (A)was employed to convert the shade tolerance estimates of North American and European species to a common scale, while theregression in (B) was employed to calibrate the East Asian species rankings.
ULO NIINEMETS AND FERNANDO VALLADARES524 Ecological MonographsVol. 76, No. 4
coexisting species do not change from seedlings to adults
(Yevstigneyev 1990, Grubb 1998, Kitajima and Bolker
2003). The five-level scale used for shade tolerance (1,
very intolerant; 2, intolerant; 3, moderately tolerant; 4,
tolerant; 5, very tolerant) corresponds approximately to
the following light availabilities expressed as percentage
of full sunlight: 1, .50%; 2, 25–50%; 3, 10–25%; 4, 5–
10%; 5, 2–5%.
We used the five-level shade tolerance scale of Baker
(1949) as the starting point for the North American
species. This shade tolerance ranking is based on actual
measurements of minimum light availability of species
location (Wiesner 1907, Zon and Graves 1911), further
modified to include a wide range of foresters’ opinions
on species biology. Because it includes a large number of
important species, it is commonly used in classifying tree
light requirements in comparative studies of life history
traits in North American tree species (Kobe et al. 1995,
Coomes and Grubb 2000, Walters and Reich 2000).
Data for nine additional data sets covering more species
and providing additional data for the species included
by Baker were used to construct a more complete and
robust data set for North America (Tables 1, 2; see
Appendix B for details).
For European species, we used the species ranking of
Ellenberg (1991), which is commonly employed to
characterize species’ potential to grow in the understory
(Niinemets and Kull 1994, Coomes and Grubb 2000,
Cornwell and Grubb 2003). Ellenberg’s ecological
indicator values for light characterize species’ natural
dispersal along the habitats of varying light availability,
and vary for woody species from values of three to nine,
giving a seven-level scale (Ellenberg 1991, Hill et al.
1999, 2000). These values are derived from actual
measurements of light availability in a species’ habitat.
To improve the shade tolerance estimates of important
European trees and increase the scope of the data set, 11
additional shade tolerance scorings were included and
cross-calibrated as detailed in Appendix B and Tables
1, 2.
For East Asian species, we used the study of
Kikuzawa (1984) augmented by the assessments of
species successional position in Koike (1988) and
Maruyama (1978) and from various comparative studies
reporting species’ successional sequence and species;
tolerance of understory shade (e.g., Kohyama 1984,
Ohsawa et al. 1986, Kikuzawa 1988, Peters 1992, 1997,
Kamijo and Okutomi 1995a, b, Ozaki and Ohsawa 1995,
Peters et al. 1995, Sumida 1995, Tanouchi and
Yamamoto 1995, Nakashizuka and Iida 1996, Tanouchi
1996, Ohsawa and Nitta 1997, Suzuki 1997, Hiroki and
Ichino 1998, Lei et al. 1998, Ke and Werger 1999,
Masaki 2002, Hiroki 2003, Ishii et al. 2003, Nanami et
al. 2004; Table 1; see Appendix B for details). The
greater woody species richness in East Asia relative to
Europe and North America, which prevents the develop-
ment of straightforward rankings of the species, and the
lack of a standard classification of shade tolerance on
this continent imposed obvious limitations to the
reliable inclusion of many Asian species in our data set.
To derive a common shade tolerance scale for North
American and European species, we used the species
present in both data sets and derived a linear regression
between the shade tolerance and the light requirement
scorings (Fig. 1A). This regression equation was
employed to convert the estimates of light requirement
of European species to the common five-level shade
tolerance scale (1, very intolerant; 5, very tolerant).
Ultimately, the different shade tolerance estimates of
species common in both data sets were averaged.
For 149 East Asian native species we obtained
corresponding shade tolerance estimates for the same
species introduced to North America and/or Europe
(Table 1). We employed linear regression analysis to test
FIG. 2. (A) Correlations between the waterlogging tolerance rankings of temperate species developed in North America andEurope, and (B) correlations between the drought tolerance ranking developed in North America and species moisture indicatorvalue developed in Europe. Data points are as described for Fig. 1A. The dashed line in (A) is for the 1:1 relationship. Theregressions in (A) and (B) were used to obtain common waterlogging and drought tolerance scales for North American andEuropean species.
November 2006 525SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
whether the five-level scale of shade tolerance developed
in the native habitat of the species corresponds to the
five-level scale developed previously for the NorthAmerican and European species. This analysis demon-
strates that both the shade tolerance scorings obtainedin species’ native and foreign locations were strongly
related with minor deviations from the 1:1 line (Fig. 1B).The final shade tolerance ranking for the East Asian
species was obtained as the mean of the shade tolerance
estimates determined in the native habitats and for thesespecies growing on other continents. This ranking was
critically revised further by Professors Kihachiro Kiku-zawa, Tohru Nakashizuka, Masahiko Ohsawa, and
Tsutom Hiura (see Acknowledgments), and we believethat the best possible shade tolerance scale for East
Asian species was obtained.
Comparative waterlogging tolerance estimates
The definitions of species’ waterlogging tolerance (i.e.,tolerance of reduced root-zone soil oxygen availabilities)
vary strongly from study to study (Bell and Johnson1974, Whitlow and Harris 1979, Bratkovich et al. 1993,
Kuhns and Rupp 2000). This large variation indefinitions is partly associated with inherent differences
in response of temperate species to waterlogging
depending on whether the waterlogging is during winter
or during the growing season, whether the water is
flowing or standing, and the degree to which soil oxygen
contents decrease and soil redox potential is altered(Bratkovich et al. 1993, Crawford 1996, Pezeshki et al.
1996, 1997). We adopt the qualitative waterloggingtolerance scale of Whitlow and Harris (1979): 5, very
tolerant (survives deep, prolonged waterlogging formore than one year); 4, tolerant (survives deep water-
logging for one growing season); 3, moderately tolerant(survives waterlogging or saturated soils for 30 consec-
utive days during the growing season); 2, intolerant
(tolerates one to two weeks of waterlogging during thegrowing season); 1, very intolerant (does not tolerate
water-saturated soils for more than a few days duringthe growing season). Although waterlogging tolerance is
often considered synonymous with flooding tolerance,we note that flooding impact in riparian ecosystems also
involves, in addition, sand/gravel depositions around the
tree base and various mechanical stresses (Naiman et al.1998, Bendix and Hupp 2000).
Waterlogging tolerance rankings for the NorthAmerican species were obtained from Bell and Johnson
(1974), Minore (1979), Whitlow and Harris (1979)revised using the data from White (1973), Barnes
(1991), Tesche (1992), Bratkovich et al. (1993), Iles
and Gleason (1994), USDA NRCS (1996), Kuhns and
TABLE 1. Studies that provided the estimates of shade tolerance for native and introduced plantson different continents.
References
Number of species
North America Europe East Asia Total
Shade tolerance rankings developed in North America for native and introduced species
Note: Data are presented as Spearman rank correlation coefficients significant at P , 0.05 or better. Ellipses (���) indicate thatfewer than five common species were available.
� The number of species for every data set is given in Table 1. All rankings increase with increasing species’ shade toleranceexcept for Wiesner (minimum light at species growth location), Jahn (light requirement), both Ellenberg and Hill et al. (lightindicator value), and Ivanov (photosynthetic compensation point); these are negatively related to shade-tolerance.
� Stange et al. (2002), Smith (2004), Dirr (2005), Morris (2005), USDA NRCS (2005).
November 2006 527SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
Asian species was critically reviewed by Professors
Kihachiro Kikuzawa, Tohru Nakashizuka , Masahiko
Ohsawa, and Tsutom Hiura (see Acknowledgments), and
the tolerance rankings were adjusted by 60.25–1.0
tolerance units for a total of 26% of species in response
to their expert suggestions.
Determination of drought tolerance rankings
Drought tolerance can be achieved by a diverse array
of structural and physiological traits, and plant rankings
according to drought tolerance are often based on
different combinations of traits and evidence. The three
major bases for species rankings are physiological
tolerance to water stress, morphological and life cycle
strategies to cope with scant water, and the water
availability estimated on the sites where the species more
robur, Q. rubra, Q. turbinella, and Q. virginiana, and for
the genus Pinus, P. albicaulis, P. aristata, P. attenuata, P.
bungeana, P. cembra, P. contorta, P. coulteri, P. echinata,
P. halepensis, P. lambertiana, P. parviflora, P. ponderosa,
P. resinosa, P. strobus, P. sylvestris, P. thunbergii, P.
virginiana, and P. wallichiana.
With the phylogenetic information of these species of
Quercus and Pinus, phylogenetic independent contrasts
(Felsenstein 1985) were carried out to remove the
influence of phylogeny on the relationships between
the tolerances to shade, drought, and waterlogging. The
software PDAP (Phenotypic Diversity Analysis Pro-
grams, Version 6.0, by T. Garland, Jr., P. E. Midford, J.
A. Jones, A. W. Dickerman, and R. Diaz-Uriarte),
which is described in Garland et al. (1993), was used.
The independent contrasts were carried out with the
module PDTREE (Garland et al. 1999). PDTREE
allows the user to enter and edit a phylogenetic tree
and associated phenotypic data for the species at its tips,
which in our case were the values of tolerance to shade,
drought, and waterlogging. Since only two phenotypic
values can be entered at each tip and node, three trees
per genus were used to estimate pairwise correlations
between the tolerances to the three environmental
factors. Branch lengths from the molecular phylogenies
of the species of Quercus and Pinus were directly taken
from the bibliography (Liston et al. 1999, Manos et al.
1999). A Brownian motion model of evolution was
assumed. Multifurcations (polytomies) were only found
for the Pinus tree and these were handled as described in
November 2006 529SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
Purvis and Garland (1993). Felsenstein’s pairwise
independent differences (contrasts) were standardized
by dividing each contrast by the standard deviation of
the contrast (i.e., square root of the sum of the lengths of
the branches of the phylogenetic tree). Correlations
between traits were also estimated in phylogenetically
independent contrasts using the AOT module of
PHYLOCOM. The significance was obtained using n
� 2 degrees of freedom in a table R, where n is the
number of internal nodes providing contrasts, because
randomization of tip values breaks down patterns of
trait conservatism (Lapointe and Garland 2001). This
approach was used for both the whole data set of species
and the species of Quercus and Pinus listed above.
Data analysis
All tolerance scales were derived from independent
observations on species’ ecological potentials and thus
satisfy the primary criterion of the statistical analysis.
The bivariate relationships between shade, drought, and
waterlogging tolerance estimates were explored by
standardized major axis regressions using the program
(S)MATR 1.0 (Falster et al. 2003). Standardized major
axis (SMA) regression estimates the residuals from the
line in both x and y dimensions (Warton and Weber
2002); SMA regression is an appropriate method for
fitting the data if the functional relationships between
the variables is not known a priori, and if both x and y
variables are measured with a certain degree of error. In
addition, SMA regressions are particularly pertinent for
comparison of bivariate relationships among groups of
data, because SMA fitting avoids flattening of the slope
as the correlation between the variables decreases
(Wright and Cannon 2001, Warton and Weber 2002).
The SMA regressions between species groups were
compared by (S)MATR 1.0 (Falster et al. 2003). This
program first uses a maximum-likelihood ratio devel-
oped by Warton and Weber (2002) to test for the slope
differences of SMA regressions. (The equivalent test in
ordinary ANCOVA is the separate slope model.)
Whenever slopes are found not to be different, the
analysis is continued according to standard ANCOVA
(common slope model) to test for difference among the
intercepts. All relationships were considered significant
at P , 0.05.
Quantile regression, a powerful technique to examine
ecological patterns (Cade and Noon 2003), was used to
explore the relationships between tolerances over the
entire surface of the scatter diagrams. Quantile regres-
sion is based on least absolute values and the model is fit
by minimizing the sum of the absolute values of the
residuals; the technique is very resistant to outliers and
allows for the exploration of relationships from the
edges of the diagrams by estimating quantiles of the
dependent variable ranging from 0% to 100% (Scharf et
al. 1998). Quantile regression was carried out with the
software Blossom, Version 2005.05.26 (Cade and
Richards 2005).
RESULTS
Tolerance scales
Ten species rankings were employed to derive the final
mean shade tolerance estimate for North American
species, while 13 shade tolerance rankings were used for
European species, and three major rankings along with a
series of detailed succession and ecophysiological studies
were used for East Asian species (Table 1). For all sets of
data, various shade tolerance scorings were strongly
correlated (Table 2 for North American and European
data sets; r ¼ 0.91 for Kikuzawa [1984] vs. East Asian
mean ranking; r¼ 0.89 for Koike [1988] vs. mean; and r
¼0.92 for Maruyama [1978] vs. mean; P , 0.001 for all),
demonstrating a strong convergence of different species’
shade tolerance rankings and the reliability of the
derived mean species value.
In addition, cross-calibration of shade tolerance scales
among different continents and available data of shade
tolerance of naturalized species on specific continents
further enhanced the reliability and extension of the data
set. Certainly, including shade tolerance estimates for
species naturalized in foreign habitats introduces some
uncertainty. In particular, exotic species may become
more tolerant in foreign habitats due to hybridization
with native species and following gene flow by intro-
gression into exotic species populations (Milne and
Abbott 2000), as well as due to selection of more
tolerant varieties by gardeners. However, we compared
the shade tolerance estimates of species in natural and
introduced habitat using paired t tests and found that
the shade tolerance in the introduced habitat did not
differ significantly from that in native habitat. For
instance, P . 0.7, for comparison of shade tolerance
estimates of North American species growing in native
habitat and in Europe.
We obtained reliable drought and waterlogging
tolerance scales for North American and European/
East Asian species using a series of revised assessments
of species’ performance (13 extensive data sets for North
America and 13 for Europe along with a series of case
studies). All data sets were strongly correlated, and
these correlations were employed to cross-calibrate the
data sets and calculate the mean tolerance estimates (see
Appendix B for the statistics). Using the mean values
effectively reduces the study-to-study bias in species’
scorings, thereby enhancing the reliability of final
tolerance estimates. Further using these cross-calibrated
mean values for species in every continent, we used
species native on several continents as well as intro-
duced species to develop global waterlogging and
drought tolerance scales (Fig. 2). As with shade
tolerance, we did not observe any statistical difference
among the drought and waterlogging tolerance esti-
mates of the species in their native and introduced
habitat (P . 0.5), suggesting that we have obtained
general and unbiased intercontinental drought and
waterlogging tolerance scales.
ULO NIINEMETS AND FERNANDO VALLADARES530 Ecological MonographsVol. 76, No. 4
Correlations between species’ shade, drought,
and waterlogging tolerances
Pooling all data, we observed negative correlations
between species’ shade and drought tolerance, shade and
waterlogging tolerance, and drought and waterlogging
tolerance (Table 3A, Figs. 3–5). The negative correla-
tions between shade and drought tolerance (Figs. 3A–C,
4A) and drought and waterlogging tolerance (Figs. 3G–
I, 4C) were significant for all continents, and a negative
correlation was also found between species’ shade and
waterlogging tolerance for the European (Fig. 3E) and
East Asian (Fig. 3F) data sets.
Due to the simultaneous negative correlations be-
tween species’ shade and waterlogging tolerance (Fig.
3E) and drought and waterlogging tolerance (Fig. 3H),
in particular for the European data set, several species
were apparently outliers in Fig. 3B. These shade
intolerant species with high waterlogging tolerance had
low drought tolerance, and interestingly, most of them
belonged to the family Ericaceae, which contains many
dominant species in raised bogs. The negative correla-
tion between species’ shade and drought tolerance was
improved when species with waterlogging tolerance
.2.5 were removed from the data set (inset in Fig. 3B
for European data set; for all data pooled, r2¼ 0.303 for
the truncated vs. r2¼ 0.082 for the entire data set; Table
3A). The role of waterlogging tolerance in the relation-
ship between shade and drought tolerance was further
assessed by linear multiple regression with all data. In
this regression, both drought (P , 0.001) and water-
logging tolerance (P , 0.001) were negatively associated
with shade tolerance (r2 ¼ 0.176).
Comparisons of the standardized major axis (SMA)
regression slopes for the relationships between shade
and drought tolerance ranked the continents according
to the slope as East Asia , North America , Europe
(Fig. 4A; P , 0.005 for comparisons between East Asian
data set with other two, and P ¼ 0.051 for the
comparison between European and North American
data sets). The East Asian data set also had significantly
more negative slope for the shade vs. waterlogging
tolerance relationship (P , 0.001). The slopes were not
different among the continents for the drought vs.
waterlogging tolerance relationship (Fig. 4C; P . 0.8),
but the elevation of the regression line was significantly
lower for the East Asian than for the North American
and European data sets (Fig. 4C; P , 0.001).
In these comparisons, the species native to both
Europe and North America (mostly species from
Ericaceae and Salicaceae families) and intercontinental
hybrids of European and North American origin, and
European and East Asian origin (n ¼ 30) were
considered as part of the European data set. When
these species with wide distribution and the interconti-
nental hybrids were considered as part of the flora of
other continents, the negative correlation between
species’ shade and waterlogging tolerance was significant
both for European (r2 ¼ 0.022, P ¼ 0.023) and North
American (r2 ¼ 0.012, P ¼ 0.039) data sets, further
TABLE 3. Bivariate relationships between shade, drought, and waterlogging tolerance estimates for 806 temperate shrub and treespecies: standardized major axis regressions.
Group
Tolerance
Intercept Slope r2 Py variable x variable
A) Species from all functional types pooled (n ¼ 806)
� Species with moderate to very high waterlogging tolerance (.2.5) were removed (n ¼ 612).� Standardized major axis (SMA) regression slopes and intercepts among different functional types were compared using the
computer program (S)MATR 1.0 (Falster et al. 2003). To compare the slopes, this software uses a maximum-likelihood ratiodeveloped by Warton and Weber (2002). When the slopes are not statistically different, the analysis is continued using standardANCOVA techniques (common slope model) to test for the difference among the intercepts (Falster et al. 2003).
November 2006 531SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
demonstrating the importance of wide distribution
Ericaceae with specific physiological potentials.
Quantile regression revealed that these negative
relationships were not always significant across the
entire scatter diagram (Fig. 5). High light species
exhibited a wide range of drought tolerances, so the
negative relationship between shade and drought
tolerance was significant only for species growing in
moderate to deep shade (Fig. 5A, D). The relationship
between shade and waterlogging tolerances was weak,
being significant only for the lowest quantiles (i.e., for
species growing in moderate shade to high light). By
contrast, the negative relationship between drought and
waterlogging tolerances was significant for all quantiles,
except for the 99% (i.e., for some exceptional species
tolerating extreme drought; Fig. 5C, F).
Functional type and tolerance to shade, drought,
and waterlogging
To determine the extent to which the correlations
between species’ ecological potentials are modified by
various functional types, we quantified the relationships
FIG. 3. Correlations between species’ shade tolerance and drought tolerance (A–C) and waterlogging tolerance (D–F), andbetween species’ drought and waterlogging tolerance (G–I) for 806 temperate woody species from North America (A, D, G; n ¼339), Europe/West Asia (B, E, H; n ¼ 256), and East Asia (C, F; n ¼ 211). Data were fitted by standardized major axis (SMA)regressions (see Table 3 for pooled regressions) using the program (S)MATR 1.0 (Falster et al. 2003), and the regressions for allcontinents are shown in Fig. 4. The statistically nonsignificant regression in (D) is shown by a dotted line. Data encircled in (B)correspond to species with high waterlogging tolerance and low drought tolerance, and the inset demonstrates the correlation for atruncated data set containing only species with waterlogging tolerance estimate ,2.5 (P , 0.001). Error bars show 6SE of separateindependent assessments for the same species. A full species list with tolerance values is provided in Appendix A.
ULO NIINEMETS AND FERNANDO VALLADARES532 Ecological MonographsVol. 76, No. 4
among tolerance estimates separately for gymnosperms
(mostly needle-leaved species in our data set, except for
Ginkgo biloba, which is a broad-leaved species) and
angiosperms (mostly broad-leaved species with the
exception of some needle-leaved species such as Erica
and Calluna from Ericaceae). These relationships were
also explored separately for evergreen and deciduous
angiosperms (mostly broad-leaved species).
Species’ shade and drought tolerance was correlated
both for gymnosperms and angiosperms (Fig. 6A, Table
3B). The slope of this relationship was significantly
greater for gymnosperms than for angiosperms (Table
3B). However, the correlations between species’ shade
and waterlogging tolerance (Fig. 6B, Table 3B) and
drought and waterlogging tolerance (Fig. 6B, Table 3B)
were significant only for angiosperms. Due to the lack of
simultaneous correlations between shade and water-
logging and drought and waterlogging tolerance, the
explained variance of shade vs. drought tolerance was
much larger for gymnosperms (r2 ¼ 0.466) than for
angiosperms (r2 ¼ 0.035).
Among the angiosperms, the slope of the shade vs.
drought tolerance relationship was not significantly
different between deciduous and evergreen broad-leaved
species, but evergreens had significantly larger shade
tolerance at a common drought tolerance (Fig. 6D,
Table 3C): For shade tolerance vs. waterlogging
tolerance, the correlations were not significantly differ-
ent among evergreen and deciduous species (Fig. 6E,
Table 3C). The slope of drought vs. waterlogging
tolerance was more negative in evergreen species (Fig.
6F, Table 3C). When the species with relatively high
waterlogging tolerance (.2.5) were removed from the
data set (mostly Ericaceae), the correlation between
shade and drought tolerance was significantly stronger
for both evergreen (n¼ 101, r2¼ 0.337, P , 0.001) and
deciduous species (n ¼ 403, r2 ¼ 0.227, P , 0.001).
Again, evergreens had a larger intercept than deciduous
species (P , 0.001), while the SMA slopes did not differ
among the groups (P . 0.8).
Simultaneous tolerance to several environmental factors
There were only a few species that were tolerant to
more than one limiting factor (tolerance index for two
variables �3). Eighty-three species (10.3% of total
species number) were both shade and drought tolerant
drought and waterlogging tolerant. There were only
three species that were tolerant to all three environ-
FIG. 4. Regressions for the correlations of (A) shadetolerance with drought tolerance, (B) shade tolerance withwaterlogging tolerance, and (C) drought tolerance with water-logging tolerance shown in Fig. 3. Insets provide the slopes ofthe standardized major axis (SMA) regressions with 95%confidence intervals (Falster et al. 2003). Slopes with the sameletter are not significantly different (P . 0.05) according to themaximum-likelihood ratio test of Warton and Weber (2002; seealso Falster et al. 2003).
November 2006 533SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
mental limitations (tolerance index for all variables �3):Amelanchier laevis, Rhododendron periclymenoides, Rho-
dodendron viscosum. Yet, the mean tolerance value
(shade, waterlogging, drought) was 3.0–3.5 for these
species, suggesting that polytolerant plants were not
very tolerant to any of these limitations.
We calculated the overall tolerance (sum of all three
indices), and the coefficients of variation (standard
deviation per sample mean) for all the tolerance
estimates and overall tolerance to further characterize
the extent of polytolerance within the entire data set.
The coefficients of variation were 0.407 for shade, 0.367
for drought, and 0.524 for waterlogging tolerance, while
the coefficient for variation for the sum of all three
tolerance indices was 0.152. This low variation in overall
tolerance further underscores the inherent trade-offs
between species’ adaptation to interacting environmen-
tal limitations and low degree of polytolerance. ‘‘Poly-
intolerance’’ was also rare, with only some genera like
Betula and Larix including species that were tolerant
neither to shade nor drought nor waterlogging.
Phylogenetic signal and influence of phylogeny on
correlations among tolerances
Phylogenetic signal, estimated as the correlation
between the phylogenetic and the tolerance matrices of
distances among species, was significant for the toler-
ance of any of the three environmental factors studied
(Table 4). Between 22% and 24% of the nodes of the
phylogenetic tree exhibited trait conservatism (i.e., stress
FIG. 5. Quantile regressions for (A) shade tolerance vs. drought tolerance, (B) shade tolerance vs. waterlogging tolerance, and(C) drought tolerance vs. waterlogging tolerance. Lines are estimates based on least absolute values for 12 quantiles (from top tobottom: 99%, 95%, 90%, 85%, 75%, 50%, 25%, 20%, 15%, 10%, 5%, and 1%). Solid lines indicate significant regressions (P , 0.001);dotted lines indicate nonsignificant regressions. Panels D–F illustrate, in a simplified way, the corresponding polygonal pattern ofeach relationship.
ULO NIINEMETS AND FERNANDO VALLADARES534 Ecological MonographsVol. 76, No. 4
tolerance was more similar among related species thanexpected by chance) and only 6–8% of the nodes
exhibited significant divergence (Table 5). Divergenceoccurred at branches closer to the root of the
phylogenetic tree than conservatism, which was ob-served in bifurcations nearer the tips (Table 5).
Phylogenetic signal was significant for the whole dataset of species, and for the 18 species of Pinus for which
we could obtain reliable phylogenetic information, but
not for the 11 species of Quercus with availablephylogenetic information. This phylogenetic signal was
generally low with the correlation coefficients (Pearson’s
r) of 0.026–0.147. The exception was shade tolerance inPinus species (r ¼ 0.404).
The inverse relationships between stress toleranceestimates were significant in phylogenetically independ-
ent contrasts carried out with the whole set of species(AOT module of PHYLOCOM). The correlations
ranged from �0.1 (drought vs. waterlogging tolerance)
to�0.37 (shade vs. drought tolerance; P , 0.01 for all).The strongest relationship was between shade and
drought, and this relationship was also significant inspecies-level phylogenetically independent contrasts in
both Pinus and Quercus (Figs. 7, 8). Among the rest of
FIG. 6. Comparison of the relationships between (A, D) shade and drought tolerance, (B, E) shade and waterlogging tolerance,and (C, F) drought and waterlogging tolerance. In panels A–C, gymnosperms (open circles) and angiosperms (solid circles) arecompared, and in panels D–F, deciduous (open circles) and evergreen (solid circles) angiosperms are compared. Data were fitted bystandardized major axis (SMA) regressions (Falster et al. 2003). The regression statistics are provided in Table 3B and C.Nonsignificant regression lines (P . 0.05) for gymnosperms in B and C are not shown. Error bars represent 6SE. Gymnospermspecies are mostly conifers, while angiosperm species are mainly broad-leaved (Appendix A).
November 2006 535SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
the pairwise inverse relationships between tolerance
estimates, only drought and waterlogging tolerance
were significantly correlated in Pinus. While significant
divergences and convergences in stress tolerance in
Quercus occurred near the tips (i.e., within sections
and subgenera), an interesting significant divergence in
drought tolerance was found in Pinus, with species of the
subgenus Pinus being more drought tolerant than
species of the subgenus Strobus (Figs. 7, 8).
DISCUSSION
Plant shade tolerance rankings
Any stress factor that decreases the ability of plants to
use available light will increase the minimum daily light
dose that the plant requires to survive under given
conditions. Therefore, there is no single minimum light
level that an individual of a particular species tolerates;
‘‘shade tolerance’’ is not an absolute but rather a relative
term (Spurr and Barnes 1980). Nutrient and water
availabilities, and air and soil temperature are poten-
tially capable of affecting shade tolerance (Tilman 1993,
Bazzaz and Wayne 1994), and they vary in gradients of
irradiance across gap–understory continuum. Thus,
species’ dispersal across light gradients is determined
by a complex interplay of various edaphic and climatic
factors. Due to this interplay of species’ minimum light
requirements with other environmental factors, reliable
relative rankings of species’ shade tolerance potentials
are invaluable in trying to understand forest develop-
ment and diversity.
We revised an extensive set of published shade
tolerance scorings, and constructed a common inter-
continental scale of shade tolerance. Surprisingly, the
shade tolerance rankings of woody species, most of
which are based on foresters’ and ecologists’ knowledge
of species behavior, and only very few on some
quantitative work on species dispersal across understory
habitats, have remained remarkably constant for more
than a century (Table 2). This general agreement of
species classification further corroborates the suggestion
that the relative light requirements of species vary
considerably less than the absolute ones.
Very few studies have tried to develop comparative
shade tolerance rankings for different continents (Peters
1997), and even these rankings are limited to a few
dominant species. For construction of the interconti-
nental shade tolerance scale, we used shade tolerance
rankings for species native on several continents (North
America/Europe) and the data of shade tolerance of
introduced species (North America/Europe/East Asia)
to cross-calibrate the shade tolerance rankings devel-
oped on different continents. Statistical tests suggested
that the shade tolerance of species did not differ
significantly in foreign and native habitats, possibly
because most species have been introduced during a
relatively short time period of 50–200 years. Further
detailed studies suggest that European introduced
species that have escaped from cultivation (such as the
tolerant to very tolerant species Acer platanoides,
tolerant to medium tolerant species Acer pseudoplatanus,
and intolerant species Rhamnus catharctica) appear to
occur in similar habitats and canopy positions as in their
respective native habitats (Webb and Kaunzinger 1993,
Kloeppel and Abrams 1995, Hoffman and Kearns 1997,
Mehrhoff et al. 2003). The same appears to be valid for
North American species such as Picea sitchensis and
Pseudotsuga menziesii widely cultivated in Europe or
Robinia pseudacacia and Symphoricarpus albus natural-
ized in Europe (Hermann 1987). A series of widespread
Asian species such as Ailanthus altissima or Lonicera
japonica also occur in similar habitats across the globe
(Hoffman and Kearns 1997, Mehrhoff et al. 2003).
TABLE 4. Phylogenetic signal estimated by the correlationbetween the phylogenetic and the tolerance matrices ofdistances among species in shade, drought, and waterloggingtolerances in the whole species data set, and in the generaQuercus and Pinus.
TABLE 5. Percentage of cladogram nodes exhibiting significant conservatism and divergence, mean divergence, and mean age forthe nodes for shade, drought, and waterlogging tolerances in the whole data set.
Tolerance
Nodes with conservatism Nodes with divergence
Number (%) Divergence (SD) Mean age� (%) Number (%) Divergence (SD) Mean age (%)
� Mean age is expressed as a percentage of maximal age, with zero representing the tips and 100% representing the root of thecladogram.
ULO NIINEMETS AND FERNANDO VALLADARES536 Ecological MonographsVol. 76, No. 4
The obtained shade tolerance scale further agrees with
global distribution patterns of species at the extremes of
the shade tolerance rankings as illustrated by Alnus,
Betula, and Salix species being in the majority of forests
among the most intolerant species, and Acer and Fagus
species typically among the most tolerant woody
components. In fact, minimum light availabilities in late
successional temperate Fagus forests are very similar
across the globe (Peters 1997), further corroborating
that F. crenata, F. grandifolia, and F. sylvatica should be
classified as very shade tolerant. These data collectively
suggest that the global shade tolerance scale we have
derived is robust.
Plant waterlogging and drought tolerance rankings
Significant negative correlation exists between air
humidity and the distance from streams and wetlands
(Chen et al. 1999), implying that the way the species
respond to gradual changes from excess to limiting
water availabilities may significantly modify forest
succession along these gradients, and in interaction with
shade tolerance determine the forest chronosequence in
any specific site with given water availability. Therefore,
extended forest gap models also use estimates of species’
drought and waterlogging tolerance to predict forest
succession (Bugmann and Cramer 1998). Reliable
estimates of species’ drought and waterlogging tolerance
FIG. 7. (A) Phylogenetically independent relationships between shade and drought tolerance, (B) shade and waterloggingtolerance, and (C) drought and waterlogging tolerance for the species of the genus Quercus represented in panel E. The data pointsare the Felsenstein’s pairwise independent contrasts (Felsenstein 1985) standardized with respect to the standard deviation of thecontrast. Nonsignificant (P . 0.05) regression lines are not shown. (D) Phylogenetically independent correlation coefficients(Pearson’s r) obtained with the PHYLOCOM analysis of trait routine (see Materials and Methods: Phylogenetic signal andphylogenetically independent contrasts). Key to abbreviations: Sh, shade; Dr, drought; Wl; waterlogging. Solid bars indicatesignificant correlations. (E) The Quercus phylogenetic tree is derived from the data in Manos et al. (1999). Arrows indicate nodes atwhich significant divergence (D) or conservatism (C) was obtained for the three tolerances.
November 2006 537SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
have been noted as primary limitations to further
development of these models (Bugmann and Solomon
1995, Bugmann and Cramer 1998). Species’ potentials to
cope with drought and waterlogging stress are often
characterized in succession models using a coarse scale
of tolerant/intolerant or by adding the gradation
intermediate (Prentice and Helmisaari 1991). Such
coarse scale assessments may be adequate for under-
standing the performance of species assemblages during
moderate stress events. More refined species rankings
may be needed to predict species’ survival during
extreme stress periods that occur only infrequently, but
that greatly influence community composition.
In this context, the assessment of stress tolerance at
the extremes becomes especially important. Even in our
detailed and uniform classification, many species tended
to aggregate at the lowest extreme of waterlogging
tolerance (e.g., Fig. 3D, G), partly because not many
species are tolerant, but also suggesting that the
resolution of the tolerance scale could be improved at
the lower range (tolerance ¼ 1, very intolerant). At the
higher end of our waterlogging tolerance scale, the
North American data set stands out as having more
species than European or East Asian data set. While
waterlogging tolerance scales specifically developed for
Europe include several species with waterlogging ranked
as 5, very tolerant (Glenz 2005), these values are
FIG. 8. (A) Phylogenetically independent relationships between shade and drought tolerance, (B) shade and waterloggingtolerance, and (C) drought and waterlogging tolerance for the species of the genus Pinus represented in panel E; data points are asdescribed in Fig. 7. Nonsignificant (P . 0.05) regressions are not shown. (D) Phylogenetically independent correlation coefficients(Pearson’s r) obtained with PHYLOCOM analysis of trait routine, as described in Fig. 7. (E) The Pinus phylogenetic tree wasobtained from the data of Liston et al (1999). Arrows indicate nodes at which significant divergence (D) or conservatism (C) wasobserved for the three tolerances.
ULO NIINEMETS AND FERNANDO VALLADARES538 Ecological MonographsVol. 76, No. 4
diminished when the data sets are cross-calibrated to a
common scale for the entire Northern Hemisphere. The
most waterlogging-tolerant trees in swamp forests in the
lowlands of cool temperate and warm temperate Europe
are Alnus glutinosa, and Populus and Salix species, while
Japanese wet forests are characterized by Alnus japonica,
Fraxinus mandshurica, Ulmus davidiana, and Salix
species. None of these forests are comparable, however,
to the extreme swamp forests of Taxodium in the
southeast United States that can be flooded all year
(Shidei 1974). Thus, the lack of very waterlogging-
tolerant species in Europe and East Asia in the cross-
calibrated rankings corresponds to reality.
As with waterlogging tolerance, many species tended
to cluster at the lower end of the cross-calibrated
drought tolerance scale (see Fig. 3A, G, for sample
graphs). Given that the climatic change scenarios predict
increasing shortage of water in certain geographic
locations, and more frequent waterlogging in other
locations (Albritton et al. 2001), it is important to
improve the resolution of this data set in the extremes.
Comparative ecophysiological studies like those of van
Splunder et al. (van Splunder et al. 1995, 1996, van
Splunder 1998) on European Salicaceae species, and
common garden experiments of Ranney and colleagues
on waterlogging tolerance of a series of North Ameri-
can, European, and East Asian Betula and Prunus
species (Ranney 1994, Ranney and Bir 1994) and
drought tolerance of Betula species (Ranney et al.
1991) provide invaluable means to fine-tune the toler-
ance rankings of closely related species and develop
reliable succession models for communities such as
riparian forests. We conclude that future comparative
ecophysiological studies are needed to refine the
resolution of drought and waterlogging scales for species
at the upper and lower limits of tolerance.
Inverse correlations between species’ ecological potentials
An inverse correlation between species’ shade and
drought tolerance has been hypothesized in several
studies (Smith and Huston 1989, Abrams 1994, Kubiske
et al. 1996), but tests of this hypothesis are conflicting.
Kubiske et al. (1996) investigated gas-exchange physiol-
ogy in six species of varying shade and drought tolerance
and found a stronger effect of drought on leaf
physiology in shade tolerant than in intolerant species.
In contrast, Sack (2004) found a similar effect of
drought on growth in 12 species of varying shade and
drought tolerance.
We observed an inverse correlation between species’
shade and drought tolerance for 806 species covering the
major dominants in North American, European/West
Asian, and East Asian temperate woody ecosystems
(Table 3A), as well as separately for every continent
(Figs. 3A–C, 4A), and plant functional type (Fig. 6A, D,
Table 3B, C), except for the evergreen angiosperms (Fig.
6D, Table 3C). This relationship had wide scatter with
significant variation of drought tolerance at a given
shade tolerance, and thus confirmed the suggestion that
the correlation between drought and shade tolerance is
not absolute (Sack 2004).
However, the large variability for all data pooled was
also associated with correlations between shade and
waterlogging tolerance (Figs. 3E, 6B, E, Table 3), and
drought and waterlogging tolerance (Figs. 3G–I, 4C,
6C, F, Table 3). The latter correlation agrees with
previous observations for tropical species (ter Steege
1994). These negative correlations essentially mean that
certain shade intolerant species, instead of being drought
tolerant were waterlogging tolerant (see Fig. 3B, E, H),
further underscoring the importance of trade-offs
among species in terms of their ecological potentials.
When species from the family Ericaceae were removed
from the global data set, the correlations were improved
significantly.
Among the different plant functional types, the
strongest correlation between shade and drought toler-
ance was for gymnosperms (Fig. 6A, Table 3B), which
did not exhibit a correlation between shade and water-
logging (Fig. 6B) and drought and waterlogging (Fig.
6C) tolerance. In fact, only Taxodium distichum was
characterized by a high degree of waterlogging toler-
ance, while Chamaecyparis thyoides, Larix gmelinii,
Pinus contorta ssp. contorta, P. elliotti, P. glabra, P.
serotina, P. sibirica, and P. sylvestris were moderately
tolerant of waterlogging. This low number of water-
logging-tolerant species in gymnosperms demonstrates
that not only the ecological and physiological trade-offs,
but also phylogeny and historical factors may constrain
the viable combinations of ecological potentials in
species.
It is striking that the correlations among species’
shade and drought tolerance and waterlogging and
drought tolerance were observed for all continents (Figs.
3, 4), and among most plant functional types. It is
further remarkable that the standardized major axis
regressions fitted to the data (Fig. 4A–C, Table 3)
differed only to a minor extent among the continents
and functional types. Part of these intercontinental and
functional type differences were associated with the
existence of a negative relationship between shade and
waterlogging tolerance in a specific subset of data,
primarily the species of Ericaceae. Despite the significant
phylogenetic signal found in the tolerance to each
environmental limitation (Table 4), the negative corre-
lations were also significant in phylogenetic independent
contrasts for species in the genera Pinus and Quercus,
particularly for the shade–drought tolerance relation-
ship (Fig. 5). All these findings support the generality of
the trade-offs in the tolerances to different limiting
factors.
Simultaneous tolerance to shade and drought
Certain species appeared to be tolerant of both
drought and shade (Appendix A), a simultaneous
tolerance that is difficult to understand given the
November 2006 539SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
conflicting requirements for efficient light capture (large
helix, and Ruscus aculeatus) that are also drought
tolerant, but competitive only in habitats with an
extended growing season. Thus, the noncorrelation
PLATE 1. Many dry, Mediterranean forests such as this one in Alto Tajo Natural Park (central Spain) exhibit a remarkablypoor understory due, at least in part, to the combination of drought and shade coupled with a short growth period imposed byextreme temperatures. Dominant canopy species are Quercus ilex and Pinus nigra, and the woody flora in shaded and dry sites isrepresented only by scattered individuals of Arctostaphylos uva-ursi and Buxus sempervirens. Photo credit: F. Valladares.
ULO NIINEMETS AND FERNANDO VALLADARES540 Ecological MonographsVol. 76, No. 4
between shade tolerance and drought tolerance observed
in this study (Sack 2004) relies on the presence of
evergreen broad-leaved species of warmer habitats.
Interestingly, only four gymnosperms, Abies firma,
Calocedrus decurrens, Taxus baccata, and Tsuga siebol-
dii, are both shade and drought tolerant; but again, these
gymnosperms are characteristic of warm temperate or
oceanic temperate forests with extended growing season.
In contrast, other shade-tolerant Abies, Picea, or Tsuga
species that dominate cool temperate forests, where the
length of growing season is similar for deciduous and
evergreen species, are not drought tolerant. This
evidence further underscores the importance of extended
growing season in simultaneous tolerance to shade and
drought. It also confirms the infrequency of polytol-
erance; none of the species in our data set was
simultaneously tolerant to drought, shade, and low
winter temperatures.
Polytolerance: rarity and possible implications
Several species that were moderately tolerant (toler-
ance value �3.0) simultaneously to several environ-
mental factors such as Acer negundo (shade/drought),
dendron periclymenoides, and Rhododendron viscosum,
with tolerance value for all characteristics �3.0) are
species with very limited invasive potential, suggesting
that polytolerance is not associated with invasiveness.
Besides, the mean tolerance value was 3.0–3.5 for these
species suggesting that polytolerant plants were not very
tolerant to any of these environmental limitations. Being
simultaneously tolerant to several environmental limi-
tations could imply a lack of full adaptation to each
particular limitation.
CONCLUSIONS
Limited and often biased information on species’
ecological potentials and scarcity of comparative in-
formation on species’ ecological potentials on different
continents has hampered the development of general
world-scale vegetation dynamic models. All temperate
forests in the Northern Hemisphere are physiognomi-
cally similar, often sharing species from the same genera
at various stages of succession (Alnus, Betula, Pinus, and
Populus in early-successional forests and Abies, Acer,
Fagus, and Picea in late-successional forests), suggesting
similar performance of temperate forests on different
continents and possibilities for common general patterns
at broad geographical scales.
With a few exceptions, the negative correlations
among shade, drought, and waterlogging tolerance were
significant for our global data set as well as within each
functional or phylogenetic group considered. These
negative correlations indicate that the number of
possible combinations of ecological potentials in a
species is limited by trade-offs between tolerance to
differing environmental limitations. In fact, and as the
data demonstrate, few species are characterized by
simultaneous tolerance to two environmental factors,
and even fewer are moderately tolerant to three
environmental factors. Although most species com-
monly cope with multiple environmental limitations,
polytolerance has not been frequently achieved during
the evolution of trees and shrubs of the Northern
Hemisphere. The trade-offs among the tolerances to
different limiting factors found here represent a con-
straint for niche differentiation of coexisting species
since they reduce the diversity of plant responses to the
many combinations of irradiance and water supply that
are found in natural ecosystems.
ACKNOWLEDGMENTS
We are grateful to Kihachiro Kikuzawa (Kyoto University,Kyoto, Japan), Tohru Nakashizuka (Research Institute forHumanity and Nature, Kyoto, Japan), Masahiko Ohsawa(University of Tokyo, Tokyo, Japan), and Tsutom Hiura(University of Hokkaido, Sapporo, Japan) for illuminatingdiscussions on succession in East Asian forests and for criticalreview of East Asian tolerance rankings. David Ackerly andPeter Grubb generously contributed many thoughtful com-ments, corrections, and suggestions on species biology. Thanksare also due to Miguel Verdu and to David Tena for help withthe phylogenetic analyses, and to Pablo Vargas for providingessential articles on molecular phylogenies of plants. Thisanalysis was partly funded by the Estonian Ministry ofEducation and Science (Grant 0182468As03), the SpanishMinistry of Education and Science (Grant RASINVCGL2004-04884-C02-02/BOS), the Spanish Council for Scien-tific Research (CSIC), and the Estonian Academy of Sciences(collaborative project between research institutions of CSICand research institutions in Estonia).
LITERATURE CITED
Aasamaa, K., and A. Sober. 2001. Hydraulic conductance andstomatal sensitivity to changes of leaf water status in sixdeciduous tree species. Biologia Plantarum 44:65–73.
Aasamaa, K., A. Sober, W. Hartung, and U. Niinemets. 2004.Drought acclimation of two deciduous tree species ofdifferent layers in a temperate forest canopy. Trees: Structureand Function 18:93–101.
Abrams, M. D. 1990. Adaptations and responses to drought inQuercus species of North America. Tree Physiology 7:227–238.
Abrams, M. D. 1994. Genotypic and phenotypic variation asstress adaptations in temperate tree species: a review ofseveral case studies. Tree Physiology 14:833–842.
Abrams, M. D., M. E. Kubiske, and S. A. Mostoller. 1994.Relating wet and dry year ecophysiology to leaf structure incontrasting temperate tree species. Ecology 75:123–133.
Acherar, M., and S. Rambal. 1992. Comparative waterrelations of four Mediterranean oak species. Vegetatio99–100:177–184.
Ackerly, D. D. 2004. ANALYSIS OF TRAITS (AOT), Version3.0: a module of PHYLOCOM, and Version 3.21 by C. O.Webb, S. Kempel, D. D. Ackerly, and S. W. Kempel. hhttp://www.phylodiversity.net/phylocomi
November 2006 541SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
Albritton, D. L., et al. 2001. Technical summary. Pages 21–83in IPCC third assessment report: contributions of IPCCworking groups. Summaries for policymakers and technicalsummaries from the three working group reports. Geneva,Switzerland. hhttp://www.epa.gov/oppeoee1/globalwarming/publications/reference/index.htmli
Anonymous. 1996. Auwalder in Sudbayern. StandortlicheGrundlagen und Bestockungsverhaltnisse im Staatswald.LWF Bericht, 9. Bayerische Landesanstalt fur Wald undForstwirtschaft, Freising.
Armstrong, J. V., and P. D. Sell. 1996. A revision of the Britishelms (Ulmus L., Ulmaceae): the historical background.Botanical Journal of the Linnean Society 120:39–50.
Baker, F. S. 1949. A revised tolerance table. Journal of Forestry47:179–181.
Barnes, B. V. 1991. Deciduous forests of North America. Pages219–344 in E. Rohrig and B. Ulrich, editors. Temperatedeciduous forests. Ecosystems of the world, 7. Elsevier,Amsterdam, The Netherlands.
Battaglia, L. L., S. A. Fore, and R. R. Sharitz. 2000. Seedlingemergence, survival and size in relation to light and wateravailability in two bottomland hardwood species. Journal ofEcology 88:1041–1050.
Battaglia, M., and J. B. Reid. 1993. Ontogenetic variation infrost resistance of Eucalyptus delegatensis R. T. Baker.Australian Journal of Botany 41:137–141.
Bazzaz, F. A., and P. M. Wayne. 1994. Coping with environ-mental heterogeneity: the physiological ecology of treeseedling regeneration across the gap–understory continuum.Pages 349–390 in M. M. Caldwell and R. W. Pearcy, editorsExploitation of environmental heterogeneity by plants.Ecophysiological processes above- and belowground. Phys-iological ecology. A series of monographs, texts, andtreatises. Academic Press, San Diego, California, USA.
Bell, D. T., and E. L. Johnson. 1974. Flood-caused treemortality around Illinois reservoirs. Transactions of theIllinois State Academy of Science 67:28–37.
Bendix, J., and C. R. Hupp. 2000. Hydrological and geo-morphological impacts on riparian plant communities.Hydrological Processes 14:2977–2990.
Blomberg, S. P., and T. Garland, Jr. 2002. Tempo and mode inevolution: phylogenetic inertia, adaptation and comparativemethods. Journal of Evolutionary Biology 15:899–910.
Blomberg, S. P., T. Garland, Jr., and A. R. Ives. 2003. Testingfor phylogenetic signal in comparative data: behavioral traitsare more labile. International Journal of Organic Evolution57:717–745.
Bratkovich, S., L. Burban, S. Katovich, C. Locey, J. Pokorny,and R. Wiest. 1993. Flooding and its effect on trees:information packet. Forest Resources Management andForest Health Protection, USDA Forest Service, Northeast-ern Area State and Private Forestry, St. Paul, Minnesota,USA. hhttp://www.na.fs.fed.us/spfo/pubs/nresource/flood/cover.htmli
Brzeziecki, B. 1995. Skale nominalne wymagan klimatycznychgatunkow drzew lesnych. (Nominal scales for climaticrequirements of forest tree species). Sylwan 139:53–65.
Brzeziecki, B., and F. Kienast. 1994. Classifying the life-historystrategies of trees on the basis of the Grimian model. ForestEcology and Management 69:167–187.
Bugmann, H., and W. Cramer. 1998. Improving the behaviourof forest gap models along drought gradients. Forest Ecologyand Management 103:247–263.
Bugmann, H. K. M., and A. M. Solomon. 1995. The use of aEuropean forest model in North America: a study ofecosystem response to climate gradients. Journal of Biogeog-raphy 22:477–484.
Burkart, M. 2001. River corridor plants (Stromtalpflanzen) inCentral European lowland: a review of a poorly understoodplant distribution pattern. Global Ecology and Biogeography10:449–468.
Burns, R. M., and B. H. Honkala. 1990. Silvics of NorthAmerica. Agricultural Handbook 654. USDA Forest Service,Washington, D.C., USA.
Cade, B. S., and B. R. Noon. 2003. A gentle introduction toquantile regression for ecologists. Frontiers in Ecology andthe Environment 1:412–420.
Cade, B. S., and J. D. Richards. 2005. User manual for Blossumstatistical software. U.S. Department of Interior, U.S.Geological Survey, Reston, Virginia, USA.
Carrion Vilches, M. A., P. Sanchez Gomez, and J. GuemesHeras. 2000. Primera aproximacion al significado taxonomi-co de la variabilidad foliar de Acer opalus gr. en la PenınsulaIberica (First approach to the taxonomic meaning of thefoliar variability of Acer opalus gr. in Iberian Peninsula).Portugaliae Acta Biologica, Series A. 19:239–248.
Castro, J., R. Zamora, J. A. Hodar, J. M. Gomez, and L.Gomez-Aparicio. 2004. Benefits of using shrubs as nurseplants for reforestation in Mediterranean mountains: a 4-yearstudy. Restoration Ecology 12:352–358.
Cavender-Bares, J., and F. A. Bazzaz. 2000. Changes indrought response strategies with ontogeny in Quercus rubra:implications for scaling from seedlings to mature trees.Oecologia 124:8–18.
Cerny, T. A., M. Kuhns, K. L. Kopp, and M. Johnson. 2002.Efficient irrigation of trees and shrubs. Utah State UniversityExtension, Logan, Utah, USA. Electronic Publishing, HG-523. hhttp://extension.usu.edu/files/gardpubs/hg523.htmli
Cescatti, A., and U. Niinemets. 2004. Sunlight capture. Leaf tolandscape. Pages 42–85 in W. K. Smith, T. C. Vogelmann,and C. Chritchley, editors. Photosynthetic adaptation.Chloroplast to landscape. Ecological Studies, 178. SpringerVerlag, Berlin, Germany.
Chaves, M. M., J. S. Pereira, J. Maroco, M. L. Rodrigues, C. P.P. Ricardo, M. L. Osorio, I. Carvalho, T. Faria, and C.Pinheiro. 2002. How plants cope with water stress in the field:photosynthesis and growth. Annals of Botany 89:907–916.
Chen, J., S. Saunders, T. Crow, R. J. Naiman, K. Brosofske, G.Mroz, B. Brookshire, and J. F. Franklin. 1999. Microclimatein forest ecosystem and landscape ecology. BioScience 49:288–297.
Cochard, H., F. Froux, S. Mayr, and C. Coutand. 2004. Xylemwall collapse in water-stressed pine needles. Plant Physiology134:401–408.
Collada, C., P. Fuentes-Utrilla, L. Gil, and M. T. Cervera.2004. Characterization of microsatellite loci in Ulmus minorMiller and cross-amplification in U. glabra Hudson and U.laevis Pall. Molecular Ecology Notes 4:731–732.
Condit, R., P. S. Ashton, N. Manokaran, J. V. LaFrankie, S. P.Hubbell, and R. B. Foster. 1999. Dynamics of the forestcommunities at Pasoh and Barro Colorado: comparing two50-ha plots. Philosophical Transactions of the Royal Societyof London. Series B, Biological Sciences 354:1739–1748.
Coomes, D. A., and P. J. Grubb. 2000. Impacts of rootcompetition in forests and woodlands: a theoretical frame-work and review of experiments. Ecological Monographs 70:171–207.
Cornwell, W. K., and P. J. Grubb. 2003. Regional and localpatterns in plant species richness with respect to resourceavailability. Oikos 100:417–428.
Crawford, R. M. M. 1996. Whole plant adaptations tofluctuating water tables. Folia Geobotanica et Phytotaxono-mica 31:7–24.
Dale, E. E., Jr., and S. Ware. 2004. Distribution of wetland treespecies in relation to a flooding gradient and backwater vs.streamside location in Arkansas, USA. Journal of the TorreyBotanical Society 131:177–186.
Dirr, M. 2005. Virtual plant tags. Steve Cissel, Green IndustryYellow Pages, Inc. hhttp://www.virtualplanttags.comi
Eissenstat, D. M., and A. Volder. 2005. The efficiency ofnutrient acquisition over the life of a root. Pages 185–220 inH. BassiriRad, editor. Nutrient acquisition by plants: an
ULO NIINEMETS AND FERNANDO VALLADARES542 Ecological MonographsVol. 76, No. 4
Ellenberg, H. 1991. Zeigerwerte der Gefaßpflanzen (ohneRubus). Pages 9–166 in H. Ellenberg, R. Dull, V. Wirth, W.Werner, and D. Paulißen, editors. Zeigerwerte von Pflanzenin Mitteleuropa. Scripta Geobotanica, 18. Erich Goltze KG,Gottingen, Germany.
Ellenberg, H. 1996. Vegetation Mitteleuropas mit den Alpen inokologischer, dynamischer und historischer Sicht. Fifthedition. Verlag Eugen Ulmer, Stuttgart, Germany.
Epron, D. 1997. Effects of drought on photosynthesis and onthe thermotolerance of photosystem II in seedlings of cedar(Cedrus atlantica and C. libani). Journal of ExperimentalBotany 48:1835–1841.
Epron, D., E. Dreyer, and G. Aussenac. 1993. A comparison ofphotosynthetic responses to water stress in seedlings from 3oak species: Quercus petraea (Matt.) Liebl., Q. rubra L. andQ. cerris L. Annales des Sciences Forestieres 50:48–60.
Falster, D. S., D. I. Warton, and I. J. Wright. 2003. (S)MATR:standardized major axis tests and routines. Version 1.0.Department of Biological Sciences, Macquarie University,Sydney, Australia. hhttp://www.bio.mq.edu.au/SMATRi
Felsenstein, J. 1985. Phylogenies and the comparative method.American Naturalist 125:1–15.
Fowells, H. A. 1965. Silvics of forest trees of the United States.Agriculture handbook, No. 271. U.S. Department ofAgriculture Forest Service, Washington, D.C., USA.
Frye, J., and W. Grosse. 1992. Growth responses to floodingand recovery of deciduous trees. Zeitschrift fur Naturfor-schung, Section C. Journal of Biosciences 47c:683–689.
Garland, T., Jr., A. W. Dickerman, C. M. Janis, and J. A.Jones. 1993. Phylogenetic analysis of covariance by computersimulation. Systematic Biology 42:265–292.
Garland, T., Jr., P. E. Midford, and A. R. Ives. 1999. Anintroduction to phylogenetically based statistical methods,with a new method for confidence intervals on ancestralstates. American Zoologist 39:374–388.
Gayer, K. 1898. Der Waldbau. vierte, verbesserte Auflageedition. Verlagsbuchhandlung Paul Parey, Berlin, Germany.
Gitay, H., and I. R. Noble. 1994. What are functional types andhow should we seek them? Pages 3–19 in T. M. Smith, H. H.Shugart, and F. I. Woodward, editors. Plant functional types.Their relevance to ecosystem properties and global change.International Geosphere–Biosphere Programme book series,1. Cambridge University Press, Cambridge, UK.
Glenz, C. 2005. Process-based, spatially-explicit modelling ofriparian forest dynamics in Central Europe—tool fordecisionmaking in river restoration. Ecole PolytechniqueFederale de Lausanne, Lausanne, France.
Graham, S. A. 1954. Scoring tolerance of forest trees.University of Michigan Research Note 4. School of NaturalResources, University of Michigan, Ann Arbor, Michigan,USA.
Grime, J. P. 1979. Plant strategies and vegetation processes.Wiley, New York, New York, USA.
Grubb, P. J. 1998. A reassessment of the strategies of plantswhich cope with shortages of resources. Perspectives in PlantEcology, Evolution and Systematics 1:3–31.
Hall, R. B. W., and P. A. Harcombe. 1998. Flooding altersapparent position of floodplain saplings on a light gradient.Ecology 79:847–855.
Harms, W. R., H. T. Schreuder, D. D. Hook, and C. L. Brown.1980. The effects of flooding on the swamp forest in LakeOcklawaha, Florida. Ecology 61:1412–1421.
Hastwell, G. T., and J. M. Facelli. 2003. Differing effects ofshade-induced facilitation on growth and survival during theestablishment of a chenopod shrub. Journal of Ecology 91:941–950.
Hermann, R. K. 1987. North American tree species in Europe.Journal of Forestry 85:27–32.
Hicks, D. J., and B. F. Chabot. 1985. Deciduous forest. Pages257–277 in B. F. Chabot and H. A. Mooney, editors.Physiological ecology of North American plant communities.Chapman and Hall, New York, New York, USA.
Hill, M. O., J. O. Mountford, D. B. Roy, and R. G. H. Bunce.1999. Ellenberg’s indicator values for British plants. Centrefor Ecology and Hydrology, Huntingdon, Cambs, UK.
Hill, M. O., D. B. Roy, J. O. Mountford, and R. G. H. Bunce.2000. Extending Ellenberg’s indicator values to a new area: analgorithmic approach. Journal of Applied Ecology 37:3–15.
Hiroki, S. 2003. Early life history stage and segregativedistribution of Fagaceae in Japan. Pages 14–14 in Integrationof silviculture and genetics in creating and sustaining oakforests. Joint meeting of IUFRO working groups. Genetics ofQuercus and improvement and silviculture of oaks. OAK2003, Tsukuba, Japan.
Hiroki, S., and K. Ichino. 1998. Comparison of growth habitsunder various light conditions between two climax species,Castanopsis sieboldii and Castanopsis cuspidata, with specialreference to their shade tolerance. Ecological Research 13:65–72.
Hoagland, B. W., L. R. Sorrels, and S. M. Glenn. 1996. Woodyspecies composition of floodplain forests of the Little River,McCurtain and LeFlore Counties, Oklahoma. Proceedings ofthe Oklahoma Academy of Science 76:23–29.
Hoffman, R., and K. Kearns. 1997. Wisconsin manual ofcontrol recommendations for ecologically invasive plants.Wisconsin Department of Natural Resources, Madison,Wisconsin, USA.
Hosner, J. F. 1958. The effects of complete inundation uponseedlings of six bottomland tree species. Ecology 39:371–373.
Hsiao, T. C. 1973. Plant responses to water stress. AnnualReview of Plant Physiology 24:519–570.
Iles, J., and M. Gleason. 1994. Understanding the effects offlooding on trees. Sustainable urban landscapes, 1. IowaState University Extension, Urbandale, Iowa, USA.hwww.extension.iastate.edu/Publications/SUL1.pdfi
Ishii, H., M. Ooishi, Y. Maruyama, and T. Koike. 2003.Acclimation of shoot and needle morphology and photosyn-thesis of two Picea species to differences in soil nutrientavailability. Tree Physiology 23:453–461.
Ivanov, L. A., and N. L. Kossovich. 1932. O raboteassimilyatsionnovo apparata drevesnyh porod. II. Botani-cheskii Zhurnal 17:3–71.
Jahn, G. 1991. Temperate deciduous forests of Europe. Pages377–502 in E. Rohrig and B. Ulrich, editors. Temperatedeciduous forests. Ecosystems of the world, 7. Elsevier,Amsterdam, The Netherlands.
Jones, R. H., and R. R. Sharitz. 1989. Potential advantages anddisadvantages of germinating early for trees in floodplainforests. Oecologia 81:443–449.
Jones, R. H., R. R. Sharitz, P. M. Dixon, D. S. Segal, and R. L.Schneider. 1994. Woody plant regeneration in four floodplainforests. Ecological Monographs 64:345–367.
Journal of Ecology. 1941–2005. The biological flora. BritishEcological Society, London, UK. hhttp://www.open.ac.uk/OU/Academic/Biology/JEcolol/Bflora.htmi
Kamijo, T., and K. Okutomi. 1995a. Distribution of Casta-nopsis forest and Persea forest and its causal factors on thesouthern part of Izu Islands. Journal of Phytogeography andTaxonomy 43:67–73.
Kamijo, T., and K. Okutomi. 1995b. Seedling establishment ofCastanopsis cuspidata var. sieboldii and Persea thunbergii onlava and scoria of the 1962 eruption on Miyake-jima Island,the Izu Islands. Ecological Research 10:235–242.
Karrenberg, S., P. J. Edwards, and J. Kollmann. 2002. The lifehistory of Salicaceace living in the active zone of floodplains.Freshwater Biology 47:733–748.
Ke, G., and M. J. A. Werger. 1999. Different responses to shadeof evergreen and deciduous oak seedlings and the effect ofacorn size. Acta Oecologica 20:579–586.
November 2006 543SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
Kikuzawa, K. 1984. Leaf survival of woody plants in deciduousbroad-leaved forests. 2. Small trees and shrubs. CanadianJournal of Botany 62:2551–2556.
Kikuzawa, K. 1988. Leaf survivals of tree species in deciduousbroad-leaved forests. Plant Species Biology 3:67–76.
King, R. A., and C. Ferris. 2002. A variable minisatellitesequence in the chloroplast genome of Sorbus L. (Rosaceae:Maloideae). Genome 45:570–576.
Kitajima, K., and B. M. Bolker. 2003. Testing performance andrank reversals among coexisting species: crossover pointirradiance analysis by Sack and Grubb (2001) and alter-natives. Functional Ecology 17:276–281.
Kloeppel, B. D., and M. D. Abrams. 1995. Ecophysiologicalattributes of the native Acer saccharum and the exotic Acerplatanoides in urban oak forests in Pennsylvania, USA. TreePhysiology 15:739–746.
Kobe, R. K., S. W. Pacala, J. A. Silander, Jr., and C. D.Canham. 1995. Juvenile tree survivorship as a component ofshade tolerance. Ecological Applications 5:517–532.
Kohyama, T. 1984. Regeneration and coexistence of two Abiesspecies dominating subalpine forests in central Japan.Oecologia 62:156–161.
Koike, T. 1988. Leaf structure and photosynthetic performanceas related to the forest succession of deciduous broad-leavedtrees. Plant Species Biology 3:77–87.
Kozlowski, T. T. 1997. Responses of woody plants to floodingand salinity. Tree physiology monograph, No. 1. HeronPublishing, Victoria, British Columbia, Canada.
Kozlowski, T. T., P. J. Kramer, and S. G. Pallardy. 1991. Thephysiological ecology of woody plants. Physiological ecol-ogy. A series of monographs, texts, and treatises. AcademicPress, San Diego, California, USA.
Kreuzwieser, J., S. Furniss, and H. Rennenberg. 2002. Impactof waterlogging on the N-metabolism of flood tolerant andnontolerant tree species. Plant, Cell and Environment 25:1039–1049.
Kubiske, M. E., and M. D. Abrams. 1994. Ecophysiologicalanalysis of woody species in contrasting temperate commun-ities during wet and dry years. Oecologia 98:303–312.
Kubiske, M. E., M. D. Abrams, and S. A. Mostoller. 1996.Stomatal and nonstomatal limitations of photosynthesis inrelation to the drought and shade tolerance of tree species inopen and understory environments. Trees: Structure andFunction 11:76–82.
Kuhns, M., and L. Rupp. 2000. Selecting and plantinglandscape trees. Electronic Publishing, NR-460. Utah StateUniversity Extension, Logan, Utah, USA. hhttp://extension.usu.edu/files/natrpubs/nr460.htmli
Lambers, H., F. S. Chapin, III, and T. L. Pons. 1998. Plantphysiological ecology. Springer Verlag, New York, NewYork, USA.
Lapointe, F. J., and T. Garland, Jr. 2001. A generalizedpermutation model for the analysis of cross-species data.Journal of Classification 18:109–127.
Larcher, W. 1994. Okophysiologie der Pflanzen. Leben,Leistung und Streßbewaltigung der Pflanzen in ihrer Umwelt.UTB fur Wissenschaft: Große Reihe, Fifth edition. VerlagEugen Ulmer, Stuttgart, Germany.
Larcher, W. 1995. Physiological plant ecology. Ecophysiologyand stress physiology of functional groups. Springer Verlag,Berlin, Germany.
Legendre, P., and L. Legendre. 1983. Numerical ecology.Elsevier, Amsterdam, The Netherlands.
Lei, T. T., R. Tabuchi, M. Kitao, K. Takahashi, and T. Koike.1998. Effects of season, weather and vertical position on thevariation in light quantity and quality in a Japanese decidousbroadleaf forest. Journal of Sustainable Forestry 6:35–55.
Liang, N., K. Maruyama, and Y. Huang. 1995. Interactions ofelevated CO2 and drought stress in gas exchange and water-use efficiency in three temperate deciduous tree species.Photosynthetica 31:529–539.
Linton, M. J., J. S. Sperry, and D. G. Williams. 1998. Limits towater transport in Juniperus osteosperma and Pinus edulis:implications for drought tolerance and regulation of transpi-ration. Functional Ecology 12:906–911.
Liston, A., W. A. Robinso, D. Pinero, and E. R. Alvarez-Buylla. 1999. Phylogenetics of Pinus (Pinaceae) based onnuclear ribosomal DNA internal transcribed spacer regionsequences. Molecular Phylogenetics and Evolution 11:95–109.
Loewenstein, N. J., and S. G. Pallardy. 1998. Droughttolerance, xylem sap abscisic acid and stomatal conductanceduring soil drying: a comparison of young plants of fourtemperate deciduous angiosperms. Tree Physiology 18:421–430.
Ludlow, M. M. 1989. Strategies of response to water stress.Pages 269–281 in K. H. Kreeb, H. Richter, and T. M.Hinckley, editors. Structural and functional responses toenvironmental stresses: water shortage. SPB AcademicPublishers, The Hague, The Netherlands.
Lusk, C. H. 2004. Leaf area and growth of juvenile temperateevergreens in low light: species of contrasting shade tolerancechange rank during ontogeny. Functional Ecology 18:820–828.
Manos, P. S., J. J. Doyle, and K. C. Nixon. 1999. Phylogeny,biogeography, and processes of molecular differentiation inQuercus subgenus Quercus (Fagaceae). Molecular Phyloge-netics and Evolution 12:333–349.
Maruyama, K. 1978. Ecological studies on natural beech forest.32. Shoot elongation characteristics and phenological behav-ior of forest trees in natural beech forest. Bulletin of theNiigata University Forests 11:1–30.
Maruyama, K., and Y. Toyama. 1987. Effect of water stress onphotosynthesis and transpiration in three tall deciduous trees.Journal of the Japanese Forest Society 69:165–170.
Masaki, T. 2002. Structure and dynamics. Pages 53–65 in T.Nakashizuka and Y. Matsumoto, editors. Diversity andinteraction in a temperate forest community—Ogawa ForestReserve of Japan. Ecological Studies, 158. Springer Verlag,Berlin, Germany.
Mediavilla, S., and A. Escudero. 2004. Stomatal responses todrought of mature trees and seedlings of two co-occurringMediterranean oaks. Forest Ecology and Management 187:281–294.
Meerow, A. W., and J. G. Norcini. 1997. Native trees for NorthFlorida. Date first printed September 1989; reviewed June1997 and October 2003. Department of EnvironmentalHorticulture, Florida Cooperative Extension Service, Insti-tute of Food and Agricultural Sciences, University ofFlorida, Gainesville, Florida, USA. hhttp://edis.ifas.ufl.edu/i
Mehrhoff, L. J., K. J. Metzler, and E. E. Corrigan. 2003. Non-native and potentially invasive vascular plants in Conneticut.Center for Conservation and Biodiversity, University ofConneticut, Storrs, Connecticut, USA.
Merritt, A. 1994. Wetlands, industry and wildlife. A manual ofprinciples and practices. The Wildfowl and Wetlands Trust,Slimbridge, Gloucester, UK.
Milne, R. I., and R. J. Abbott. 2000. Origin and evolution ofinvasive naturalized material of Rhododendron ponticum L. inthe British Isles. Molecular Ecology 9:541–556.
Minore, D. 1979. Comparative autecological characteristics ofnorthwestern tree species: a literature review. USDA ForestService Technical Report, PNW-87. Pacific Northwest Forestand Range Experiment Station, Portland, Oregon, USA.
Miyazawa, Y., and K. Kikuzawa. 2005. Winter photosynthesisby saplings of evergreen broadleaved trees in a deciduoustemperate forest. New Phytologist 165:857–866.
ULO NIINEMETS AND FERNANDO VALLADARES544 Ecological MonographsVol. 76, No. 4
Mooney, H. A., F. S. Chapin, III, and P. A. Matson. 2002.Principles of terrestrial ecosystem ecology. Springer Verlag,New York, New York, USA.
Mooney, H. A., and R. J. Hobbs. 2000. Invasive species in achanging world. Island Press, Washington, D.C., USA.
Morozov, G. F. 1903. Forest dendrology. Attitude of treespecies to light. On the types of of tree stands. A conspectusof lectures. Lesnoi Institute, St. Peterburg, Russia.
Morris, R., editor. 2005. Plants for a future. Edible medicinaland useful plants for a healthier world. Plants for a FutureFoundation. Charity No. 1057719, Lerryn, Lostwithiel,Cornwall, PL22 0QJ. hhttp://pfaf.org/i
Naiman, R. J., K. L. Fetherston, S. McKay, and J. Chen. 1998.Riparian forests. Pages 289–323 in R. J. Naiman and E.Bilby, editors. River ecology and management: lessons fromthe Pacific coastal ecoregion. Springer Verlag, New York,New York, USA.
Nakashizuka, T., and S. Iida. 1996. Composition, dynamicsand disturbance regime of temperate deciduous forests inmonsoon Asia. Pages 23–30 in T. Hirose, B. H. Walker, H. A.Mooney, and A. Kratochwil, editors Global change andterrestrial ecosystems in monsoon Asia. Tasks for vegetationscience. Kluwer Academic Publishers, Dordrecht, TheNetherlands.
Nanami, S., H. Kawaguchi, R. Tateno, C. Li, and S. Katagiri.2004. Sprouting traits and population structure of co-occurring Castanopsis species in an evergreen broad-leavedforest in southern China. Ecological Research 19:341–348.
Ni, B.-R., and S. G. Pallardy. 1991. Response of gas exchangeto water stress in seedlings of woody angiosperms. TreePhysiology 8:1–9.
Niinemets, U., and K. Kull. 1994. Leaf weight per area and leafsize of 85 Estonian woody species in relation to shadetolerance and light availability. Forest Ecology and Manage-ment 70:1–10.
Niinemets, U., and O. Kull. 1998. Stoichiometry of foliarcarbon constituents varies along light gradients in temperatewoody canopies: implications for foliage morphologicalplasticity. Tree Physiology 18:467–479.
Niinemets, U., and F. Valladares. 2004. Photosyntheticacclimation to simultaneous and interacting environmentalstresses along natural light gradients: optimality andconstraints. Plant Biology 6:254–268.
Nikolov, N., and H. Helmisaari. 1992. Silvics of the circum-polar boreal forest tree species. Pages 13–84 inH. H. Shugart,R. Leemans, and G. B. Bonan, editors. A system analysis ofthe global boreal forest. Cambridge University Press, Cam-bridge, UK.
Oberdorfer, E., T. Muller, D. Korneck, W. Lippert, E. Patzke,and H. E. Weber. 1994. Pflanzensoziologische Exkursions-flora. UTB fur Wissenschaft: Uni-Taschenbucher, 1828,Seventh edition. Verlag Eugen Ulmer, Stuttgart, Germany.
Ohsawa, M., and I. Nitta. 1997. Patterning of subtropical/warm-temperate evergreen broad-leaved forests in East Asianmountains with special reference to shoot phenology. Tropics6:317–334.
Ohsawa, M., P. R. Shakya, and M. Numata. 1986. Distributionand succession of west Himalaya forest types in the easternpart of the Nepal Himalaya. Mountain Research andDevelopment 6:143–157.
Otto, H.-J. 1994. Waldokologie. Verlag Eugen Ulmer, Stutt-gart, Germany.
Ozaki, K., and M. Ohsawa. 1995. Successional change of forestpattern along topographical gradients in warm-temperatemixed forests in Mt. Kiyosumi, central Japan. EcologicalResearch 10:223–234.
Peng, C. H. 2000. From static biogeographical model todynamic global vegetation model: a global perspective onmodelling vegetation dynamics. Ecological Modelling 135:33–54.
Percival, G. C., and C. N. Sheriffs. 2002. Identification ofdrought-tolerant woody perennials using chlorophyll fluo-rescence. Journal of Arboriculture 28:215–222.
Peters, R. 1992. Ecology of beech forests in the NorthernHemisphere. Dissertation. Landbouwuniversiteit Wagenin-gen, The Netherlands.
Peters, R. 1997. Beech forests. Geobotany. Kluwer AcademicPublishers, Dordrecht, The Netherlands.
Peters, R., H. Tanaka, M. Shibata, and T. Nakashizuka. 1995.Light climate and growth in shade-tolerant Fagus crenata,Acer mono and Carpinus cordata. Ecoscience 2:67–74.
Pezeshki, S. R., R. D. DeLaune, and J. F. Meeder. 1997.Carbon assimilation and biomass partitioning in Avicenniagerminans and Rhizophora mangle seedlings in response tosoil redox conditions. Environmental and ExperimentalBotany 37:161–171.
Pezeshki, S. R., J. H. Pardue, and R. D. DeLaune. 1996. Leafgas exchange and growth of flood-tolerant and flood-sensitive tree species under low soil redox conditions. TreePhysiology 16:453–458.
Pilgrim, E. S., M. J. Crawley, and K. Dolphin. 2004. Patterns ofrarity in the native British flora. Biological Conservation 120:165–174.
Prentice, I. C., and H. Helmisaari. 1991. Silvics of North-European trees: compilation, comparisons and implicationsfor forest succession modelling. Forest Ecology and Manage-ment 42:79–93.
Press, M. C. 1999. Research review. The functional significanceof leaf structure: a search for generalizations. New Phytol-ogist 143:213–219.
Purvis, A., and T. Garland, Jr. 1993. Polytomies in comparativeanalyses of continuous data. Systematic Biology 42:569–575.
Qian, H., and R. E. Ricklefs. 1999. A comparison of thetaxonomic richness of vascular plants in China and theUnited States. American Naturalist 154:160–181.
Qian, H., and R. E. Ricklefs. 2000. Large-scale processes andthe Asian bias in species diversity of temperate plants. Nature407:180–182.
Rackham, O. 2003. Ancient woodland: its history, vegetationand uses in England. Second edition. Castlepoint Press,Dalbeattie, UK.
Randall, J. M., and J. Marinelli. 1996. Invasive plants, weeds ofthe global garden. Brooklyn Botanical Garden, New York,New York, USA.
Ranney, T. G. 1994. Differential tolerance of eleven Prunustaxa to root zone flooding. Journal of EnvironmentalHorticulture 12:138–141.
Ranney, T. G., and R. E. Bir. 1994. Comparative floodtolerance of birch rootstocks. Journal of the AmericanSociety for Horticultural Science 119:43–48.
Ranney, T. G., R. E. Bir, and W. A. Skroch. 1991.Comparative drought resistance among six species of birch(Betula): influence of mild water stress on water relations andleaf gas exchange. Tree Physiology 8:351–360.
Reich, P. B., I. J. Wright, J. Cavender-Bares, J. M. Craine, J.Oleksyn,M.Westoby, andM. B.Walters. 2003. The evolutionof plant functional variation: traits, spectra and strategies.International Journal of Plant Sciences 164:s143–164.
Richens, R. 1980. On fine distinctions in Ulmus L. Taxon 29:305–312.
Ricklefs, R. E., H. Qian, and P. S. White. 2004. The regioneffect on mesoscale plant species richness between easternAsia and eastern North America. Ecography 27:129–136.
Robertson, A., A. C. Newton, and R. A. Ennos. 2004. Multiplehybrid origins, genetic diversity and population geneticstructure of two endemic Sorbus taxa on the Isle of Arran,Scotland. Molecular Ecology 13:123–134.
Sack, L. 2004. Responses of temperate woody seedlings toshade and drought: do trade-offs limit potential nichedifferentiation? Oikos 107:107–127.
November 2006 545SHADE, DROUGHT, AND WATERLOGGING TOLERANCE
Sack, L., and P. J. Grubb. 2002. The combined impacts of deepshade and drought on the growth and biomass allocation ofshade tolerant woody seedlings. Oecologia 131:175–185.
Sack, L., P. J. Grubb, and T. Maranon. 2003. The functionalmorphology of juvenile plants tolerant of strong summerdrought in shaded forest understories in southern Spain.Plant Ecology 168:139–163.
Sakio, H. 2003. Effects of flooding on the growth of seedlings ofsome deciduous tree species. Page 6 in Integration ofsilviculture and genetics in creating and sustaining oakforests. Joint meeting of IUFRO working groups. Geneticsof Quercus and improvement and silviculture of oaks. OAK2003, Tsukuba, Japan.
Sanchez-Gomez, D., F. Valladares, and M. A. Zavala. 2006a.Performance of seedlings of Mediterranean woody speciesunder experimental gradients of irradiance and wateravailability: trade-offs and evidence for niche differentiation.New Phytologist 170:795–806.
Sanchez-Gomez, D., M. A. Zavala, and F. Valladares. 2006b.Survival responses to irradiance are differentially influencedby drought in seedlings of forest tree species of the temperate-Mediterranean transition zone. Acta Oecologica, in press.
Schaffrath, J. 2000. Auswirkungen des extremen Sommerhoch-wassers des Jahres 1997 auf die Geholzwegetation in derOderaue bei Frakfurt (O.). Naturschutz und Landespflege inBrandenburg 9:4–13.
Scharf, F. S., F. Juanes, and M. Sutherland. 1998. Inferringecological relationships from the edges of scatter diagrams:comparison of regression techniques. Ecology 79:448–460.
Schmidt, M., and A. W. Schneider-Poetsch. 2002. Theevolution of gymnosperms redrawn by phytochrome genes:the Gnetatae appear at the base of gymnosperms. Journal ofMolecular Evolution 54:715–724.
Shidei, T. 1974. Forest vegetation zones. Pages 87–124 in M.Numata, editor. The flora and vegetation of Japan.Kodansha, Tokyo, Japan.
Siebel, H. N., and C. W. P. M. Blom. 1998. Effects of irregularflooding on the establishment of tree species. Acta BotanicaNeerlandica 47:231–240.
Siebel, H. N., M. v. Wijk, and C. W. P. M. Blom. 1998. Cantree seedlings survive increased flood levels of rivers? ActaBotanica Neerlandica 46:219–230.
Silvertown, J., M. Dodd, and D. Gowing. 2001. Phylogeny andthe niche structure of meadow plant communities. Journal ofEcology 79:448–460.
Smith, J. K., editor. 2004. Fire effects information system(FEIS). FEIS plants species reviews. U.S. Department ofAgriculture, Forest Service, Rocky Mountain ResearchStation, Fire Sciences Laboratory, Missoula, Montana,USA. hhttp://www.fs.fed.us/database/feisi
Smith, T., and M. Huston. 1989. A theory of the spatial andtemporal dynamics of plant communities. Vegetatio 83:49–69.
Sokal, R. R., and F. J. Rohlf. 1995. Biometry. The principlesand practice of statistics in biological research. Third edition.W. H. Freeman, New York, New York, USA.
Soltis, D. E., et al. 2000. Angiosperm phylogeny inferred from18S rDNA, rbcL, and atpB sequences. Botanical Journal ofthe Linnean Society 133:381–461.
Sperry, J. S., K. L. Nichols, J. E. M. Sullivan, and S. E.Eastlack. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interiorAlaska. Ecology 75:1736–1752.
Spurr, S. H., and B. V. Barnes. 1980. Forest ecology. Thirdedition. John Wiley and Sons, Toronto, Canada.
Stange, C., D. Ogle, and L. St. John. 2002. Tree planting, careand management. USDA Natural Resources ConservationService Technical Notes, 42. USDA NRCS, Boise, Idaho,USA
Streng, D. R., J. S. Glitzenstein, and P. A. Harcombe. 1989.Woody seedling dynamics in an East Texas floodplain forest.Ecological Monographs 59:177–204.
Sumida, A. 1995. Three-dimensional structure of a mixedbroad-leaved forest in Japan. Vegetatio 119:67–80.
Suzuki, E. 1997. The dynamics of old Cryptomeria japonicaforest on Yakushima Island. Tropics 6:421–428.
Takahashi, K., Y. Fujimura, and T. Koike. 1988. Tolerance ofdeciduous broad-leaved trees in Hokkaido to flooding. II.Seasonal change of the tolerance. Transactions of the meetingin Hokkaido branch of the Japanese Forestry Society 36:99–101.
Talbot, R. J., and J. R. Etherington. 1987. Comparative studiesof plant growth and distribution in relation to waterlogging.XIII. The effect of Fe2þ on photosynthesis and respiration ofSalix caprea and S. cinerea ssp. oleifolia. New Phytologist105:575–583.
Tanouchi, H. 1996. Survival and growth of two coexistingevergreen oak species after germination under different lightconditions. International Journal of Plant Sciences 157:516–522.
Tanouchi, H., and S. Yamamoto. 1995. Structure andregeneration of canopy species in an old-growth evergreenbroad-leaved forest of Aya district, southwestern Japan.Vegetatio 117:51–60.
Tapper, P.-G. 1993. The replacement of Alnus glutinosa byFraxinus excelsior during succession related to regenerativedifferences. Ecography 16:212–218.
Tapper, P.-G. 1996. Tree dynamics in a successional Alnus–Fraxinus woodland. Ecography 19:237–244.
Terazawa, K., and K. Kikuzawa. 1994. Effects of flooding onleaf dynamics and other seedling responses in flood-tolerantAlnus japonica and flood-intolerant Betula platyphylla var.japonica. Tree Physiology 14:251–261.
ter Steege, H. 1994. Flooding and drought tolerance in seedsand seedlings of two Mora species segregated along a soilhydrological gradient in the tropical rain forest of Guyana.Oecologia 100:356–367.
Tesche, M. 1992. Klimaresistenz. Pages 279–306 inH. Lyr, H. J.Fiedler, and W. Tranquillini, editors. Physiologie undOkologie der Geholze. Gustav Fischer Verlag, Jena, Ger-many.
Tilman, D. 1988. Plant strategies and the dynamics andstructure of plant communities. Monographs in populationbiology, 26. Princeton University Press, Princeton, NewJersey, USA.
Tilman, D. 1993. Community diversity and succession: the rolesof competition, dispersal, and habitat modification. Pages327–344 in E.-D. Schulze and H. A. Mooney, editors.Biodiversity and ecosystem function. Ecological studies, 99.Springer Verlag, Berlin, Germany.
Timmermann, G. 1992. Rosa L. 1753. Pages 64–101 in O.Sebald, S. Seybold, and G. Philippi, editors. Die Farn- undBlutenpflanzen Baden-Wurttembergs. Verlag Eugen Ulmer,Stuttgart, Germany.
Tschaplinski, T. J., G. M. Gebre, and T. L. Shirshac. 1998.Osmotic potential of several hardwood species as affected bymanipulation of throughfall precipitation in an upland oakforest during a dry year. Tree Physiology 18:291–298.
Tsukahara, H. 1985. Studies of the flood tolerance of some treespecies. Bulletin of the Yamagata University, AgriculturalScience 9:425–448.
Tyree, M. T., and J. D. Alexander. 1993. Hydraulic con-ductivity of branch junctions in three temperate tree species.Trees: Structure and Function 7:156–159.
USDA NRCS. 1996. Chapter 16. Streambank and shorelineprotection. In National engineering field handbook, Part 650.U.S. Department of Agriculture, Natural Resources Con-servation Service, Washington, D.C., USA.
USDA NRCS. 2005. The PLANTS Database, Version 3.5.Data compiled from various sources by Mark W. Skinner.National Plant Data Center, Information TechnologyCenter, Baton Rouge, Louisiana, USA. hhttp://plants.usda.govi
ULO NIINEMETS AND FERNANDO VALLADARES546 Ecological MonographsVol. 76, No. 4
Vaga, A., et al., editors. 1960. Eesti NSV floora. Eesti RiiklikKirjastus/Valgus, Tallinn, Estonia.
Valladares, F. 2003. Light heterogeneity and plants: fromecophysiology to species coexistence and biodiversity. Pages439–471 in K. Esser, U. Luttge, W. Beyschlag, and F.Hellwig, editors. Progress in botany. Springer Verlag, Berlin,Germany.
Valladares, F., S. Arrieta, I. Aranda, D. Lorenzo, D. Tena, D.Sanchez-Gomez, F. Suarez, and J. A. Pardos. 2005a. Shadetolerance, photoinhibition sensitivity and phenotypic plasti-city of Ilex aquifolium in continental-Mediterranean sites.Tree Physiology 25:1041–1052.
Valladares, F., I. Dobarro, D. Sanchez-Gomez, and R. W.Pearcy. 2005b. Photoinhibition and drought in Mediterra-nean woody saplings: scaling effects and interactions in sunand shade phenotypes. Journal of Experimental Botany 56:483–494.
Valladares, F., and R. W. Pearcy. 1997. Interactions betweenwater stress, sun–shade acclimation, heat tolerance andphotoinhibition in the sclerophyll Heteromeles arbutifolia.Plant, Cell and Environment 20:25–36.
Valladares, F., and R. W. Pearcy. 2002. Drought can be morecritical in the shade than in the sun: a field study of carbongain and photo-inhibition in a Californian shrub during a dryEl Nino year. Plant, Cell and Environment 25:749–759.
van Splunder, I. 1998. Floodplain forest recovery. Softwooddevelopment in relation to hydrology, riverbank morphologyand management. Dissertation. Katholieke Universiteit,Nijmgen, Japan.
van Splunder, I., H. Coops, L. A. C. J. Voesenek, and C. W. P.M. Blom. 1995. Establishment of alluvial forest species infloodplains: the role of dispersal timing, germinationcharacteristics and water-level fluctuations. Acta BotanicaNeerlandica 44:269–278.
van Splunder, I., L. A. C. J. Voesenek, H. Coops, X. J. A. deVries, and C. W. P. M. Blom. 1996. Morphological responsesof seedlings of four species of Salicaceae to drought.Canadian Journal of Botany 74:1988–1995.
Walter, H. 1968. Die Vegetation der Erde in oko-physiolo-gischer Betrachtung. G. Fischer, Stuttgart, Germany.
Walters, M. B., and P. B. Reich. 2000. Seed size, nitrogensupply, and growth rate affect tree seedling survival in deepshade. Ecology 81:1887–1901.
Warming, E. 1909. Oecology of plants. An introduction to thestudy of plant communities. Oxford University Press,Oxford, UK.
Warton, D. I., and N. C. Weber. 2002. Common slope tests forbivariate errors-in variables models. Biometrical Journal 44:161–174.
Webb, S. L., and C. K. Kaunzinger. 1993. Biological invasionof the Drew University (New Jersey) Forest Preserve by
Norway maple (Acer platanoides L.). Bulletin of the TorreyBotanical Club 120:334–343.
Westoby, M. 1999. Generalization in functional plant ecology:the species sampling problem, plant ecology strategyschemes, and phylogeny. Pages 847–872 in F. I. Pugnaireand F. Valladares, editors. Handbook of functional plantecology. Marcel Dekker, New York, New York, USA.
White, P. S. 1983. Corner’s rules in eastern deciduous trees:allometry and its implications for the adaptive architecture oftrees. Bulletin of the Torrey Botanical Club 110:203–212.
White, R. M. 1973. Plant tolerance for standing water: anassessment. Cornell Plantations 28:50–52.
Whitley, R. E., S. Black-Samuelsson, and D. Clapham. 2003.Development of microsatellite markers for the Europeanwhite elm (Ulmus laevis Pall.) and cross-species amplificationwithin the genus Ulmus. Molecular Ecology Notes 3:598–600.
Whitlow, T. H., and R. W. Harris. 1979. Flood tolerance inplants: a state-of-the-art review. National Technical Infor-mation Service, U.S. Deptartment of Commerce, Washing-ton, D.C., USA.
Wiesner, J. 1907. Der Lichtgenuss der Pflanzen. Photometrischeund physiologische Untersuchungen mit besonderer Ruck-sichtnahme auf Lebensweise, geographische Verbreitung undKultur der Pflanzen. Verlag von Wilhelm Engelmann,Leipzig, Germany.
Woodward, F. I. 1990. From ecosystems to genes: theimportance of shade tolerance. Trends in Ecology andEvolution 5:111–114.
Wright, I. J., and K. Cannon. 2001. Relationships between leaflifespan and structural defences in a low-nutrient, sclerophyllflora. Functional Ecology 15:351–359.
Yamamoto, F., T. Sakata, and K. Terazawa. 1995. Physio-logical, morphological and anatomical responses of Fraxinusmandshurica seedlings to flooding. Tree Physiology 15:713–719.
Yevstigneyev, O. I. 1990. Fitotsenotipy i otnosheniye listvennyhderevyev k svetu. (Phytocoenotypes and the behaviour ofdeciduous trees with respect to light.) Dissertation. Moskov-skii Gosudarstvennyi Pedagogicheskii Institut imeni V. I.Lenina, Moscow, Russia.
Yin, Y., J. C. Nelson, G. V. Swenson, H. A. Langrehr, and T.A. Blackburn. 1994. Tree mortality in the upper Mississippiriver and floodplain following an extreme flood in 1993.Pages 41–60 in Long term resource monitoring program,1993 flood observations. National Biological Service, Envi-ronmental Management Technical Center, Onalaska, Wis-consin, USA.
Zon, R., and H. S. Graves. 1911. Light in relation to treegrowth. U.S. Department of Agriculture, Forest Service,Bulletin 92. Government Printing Office, Washington, D.C.,USA.
APPENDIX A
A table showing shade, drought, and waterlogging tolerance for 806 species of woody plants from the temperate NorthernHemisphere (Ecological Archives M076-020-A1).
APPENDIX B
Additional details on the protocol followed and the original sources used to build the tolerance data set and to standardize therankings of tolerance obtained from different sources and for species from different continents (Ecological Archives M076-020-A2).
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